Social learning and its role in anti-predator behaviour by coral reef fishes

Manassa, Rachel Penelope (2013) Social learning and its role in anti-predator behaviour by coral reef fishes. PhD thesis, James Cook University.

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The lifetime fitness of a prey is directly affected by its ability to detect and avoid predators. However, predator avoidance is costly as it reduces the time and energy available for other fitness related activities. Prey must therefore continually modify and update their behaviour towards predators through the process of learning. As a variety of information sources are available to individuals at any one time, knowledge on how animals make decisions is essential for our understanding of animal behaviour. Often an individual's decisions are affected by the presence of others. This thesis investigates the importance of social interactions to the assessment of predation risk, using coral reef fish as model organisms.

Ignoring accurate information on predation risk could lead to death; therefore prey individuals are likely to have evolved the ability to incorporate multiple sources of information, extract important components and respond accordingly. Chapter 2 explored how juvenile reef fish incorporate multiple sources of information to mediate their risk response and how information sources are prioritised. Naïve anemonefish (Amphiprion percula) were exposed to damage-released chemical cues of conspecifics and closely related congenerics (Amphiprion melanopus), along with additional control cues in the presence and absence of a shoal (conspecifics, congenerics or no shoal). A. percula responded with anti-predator behaviour to the chemical cues from both conspecifics and congenerics, with visual cues dramatically influencing the response elicited. These findings emphasise the ability of coral reef fish to incorporate multiple sources of information into their decision making process, allowing individuals to reduce any uncertainty.

Information can be gained through the process of social learning, where less experienced individuals learn from observing and/or interacting with experienced group members. Chapter 3 examined the role of social learning in predator recognition in relation to the survival of newly settled juvenile reef fish. Naïve damselfish (Pomacentrus wardi) were tested for their ability to socially transmit the recognition of a predator odour to conspecifics. Along with this, the study also determined whether there was a difference in the rate of survival between individuals that directly learnt the predator odour and those who acquired the information through social learning. Results showed that P. wardi are capable of using social learning to transmit information, with the survival outcome not significantly different from those who directly experienced predator conditioning. As such, this study demonstrates that experience plays a vital role in the outcome of predator-prey interactions, with social learning improving the ability of prey to avoid and/or escape predation.

In a natural setting social learning is likely to occur between more than 2 individuals, as such investigating the effect that group size has on the learning process is vital. Chapter 4 determined the effect of group size on the ability of the damselfish, Pomacentrus amboinensis to socially learn to recognise an unknown predator. Specifically, individuals were tested to see if social learning occurred when the number of less experienced individuals (observers) was increased from 1 to 5, and if the intensity of the anti-predator response differed depending on the size of the group. Regardless of group size, P. amboinensis individuals were capable of socially transmitting the recognition of an unknown predator to conspecifics, with the intensity of the response not significantly different between predator-naïve observers who learnt when they were alone compared to when they were one of five observers. Social learning is therefore an important method of acquiring information about predators in aquatic ecosystems, ensuring that the value of the information is transferred in its entirety.

Along with intraspecific social learning (transmission of information between conspecifics), interspecific social learning (transmission of information between species) is likely to be commonplace in biologically complex environments such as coral reefs. Therefore, Chapter 5 tested if social learning of predator recognition occurs among three species of coral reef fishes. Individuals of both Pomacentrus moluccensis and Apogon trimaculatus were tested for their ability to socially learn from P. wardi. Based on a single conditioning event, individuals of both species were able to learn a predator's identity from experienced P. wardi individuals. This ability to utilise social information from heterospecifics is likely to confer a significant survival advantage, especially for coral reef fishes as they are faced with constant and unpredictable predation pressures.

Predation pressure is highest during critical life history transitions where the suite of predators one encounters is both diverse and variable. For coral reef fishes, one of the most significant transitions occurs following a planktonic larval stage; settlement into a benthic life. As this stage occurs at night, Chapter 6 explored whether social learning of predator recognition can occur in total darkness. Results demonstrated that predator-naïve anemonefish, A. percula, are capable of socially learning to recognise a novel predator when paired with a predator-experienced conspecific under both light and dark conditions. These results show that visual cues are unlikely to be the sole sensory system responsible, therefore, the study also tested whether when threatened individuals release chemical cues known as disturbance cues into the water. A. percula did release disturbance cues following exposure to predator odour; however these cues did not facilitate learnt recognition. It is likely that another sensory modality, possibly mechano-sensory in origin, is responsible for information transfer in the dark, with this study highlighting the diversity of sensory cues available to coral reef fishes.

This thesis demonstrates the use of social learning as an anti-predator mechanism, highlighting the importance of olfactory cues for predator recognition in biologically complex ecosystems. Obtaining accurate information on local predator identities is essential to the decision process of individuals, with the choices made ultimately determining the outcome of predator-prey interactions. Furthermore, this study demonstrates the speed with which information can spread through a local prey population without a dilution of importance; highlighting the role of social interactions in the cognitive processes of coral reef fishes.

Item ID: 40088
Item Type: Thesis (PhD)
Keywords: amphibian percula; amphiprion; anemonefish; apogon; behavior; behaviour; behavioural ecology; clown anemonefish; clown fish; cognition; community ecology; complex ecosystems; coral reef fish; coral reef fishes; disturbance cues; group size; learning; olfactory cue; orange clownfish; phylogenetic relatedness; pomacentridae; predation risk; predation; predator recognition; predator; predator-prey; predatory marine animals; predatory; prey; reef fishes; risk assessment; shoaling; social learning; sociality; survival; visual cues; visual information
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Manassa, R.P., Dixson, D.L., McCormick, M.I., and Chivers, D.P. (2013) Coral reef fish incorporate multiple sources of visual and chemical information to mediate predation risk. Animal Behaviour, 86 (4). pp. 717-722.

Chapter 3: Manassa, R.P., and McCormick, M.I. (2013) Social learning improves survivorship at a life-history transition. Oecologia, 171 (4). pp. 845-852.

Chapter 4: Manassa, R.P., McCormick, M.I., Dixson, D.L., Ferrari, M.C.O., and Chivers, D.P. (2014) Social learning of predators by coral reef fish: does observer number influence acquisition of information? Behavioral Ecology and Sociobiology, 68 (8). pp. 1237-1244.

Chapter 5: Manassa, R.P., McCormick, M.I., and Chivers, D.P. (2013) Socially acquired predator recognition in complex ecosystems. Behavioral Ecology and Sociobiology, 67 (7). pp. 1033-1040.

Chapter 6: Manassa, R.P., McCormick, M.I., Chivers, D.P., and Ferrari, M.C.O. (2013) Social learning of predators in the dark: understanding the role of visual, chemical and mechanical information. Proceedings of the Royal Society of London Series B, Biological Sciences, 280 (1765). pp. 1-8.

Appendix 1: Ferrari, Maud C.O., Manassa, Rachel P., Dixson, Danielle L., Munday, Philip L., McCormick, Mark I., Meekan, Mark G., Sih, Andrew, and Chivers, Douglas P. (2012) Effects of ocean acidification on learning in coral reef fishes. PLoS ONE, 7 (2). pp. 1-10.

Appendix 2: Simpson, Stephen D, Munday, Philip, Wittenrich, Matthew, Manassa, Rachel, Dixson, Danielle, Gagliano, Monica, and Yan, Hong Y (2011) Ocean acidification erodes crucial auditory behaviour in a marine fish. Biology Letters, 7 (6). pp. 917-920.

Other publications:

Manassa, R.P., and McCormick, M.I. (2012) Risk assessment via predator diet cues in a coral reef goby. Journal of Experimental Marine Biology and Ecology, 426-427. pp. 48-52.

Manassa, R.P., and McCormick, M.I. (2012) Social learning and acquired recognition of a predator by a marine fish. Animal Cognition, 15 (4). pp. 559-565.

McCormick, M. I., and Manassa, R. (2008) Predation risk assessment by olfactory and visual cues in a coral reef fish. Coral Reefs, 27 (1). pp. 105-113.

Date Deposited: 03 Sep 2015 02:01
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060202 Community Ecology (excl Invasive Species Ecology) @ 50%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 50%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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